Benign Convulsions with Mild Rotavirus and Norovirus Gastroenteritis: Nationwide Data from the Health Insurance Review and Assessment Service in ...
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
children Article Benign Convulsions with Mild Rotavirus and Norovirus Gastroenteritis: Nationwide Data from the Health Insurance Review and Assessment Service in South Korea Dong Hyun Kim † , Dong Jun Ha † , Yeong Seok Lee , Min Jun Chun and Young Se Kwon * Department of Pediatrics, Inha University School of Medicine, Incheon 22332, Korea; id@inha.ac.kr (D.H.K.); djha0917@inhauh.com (D.J.H.); yslee1016@inhauh.com (Y.S.L.); mjchun0716@inhauh.com (M.J.C.) * Correspondence: ysped@inha.ac.kr; Tel.: +82-32-890-3579 † These authors contributed equally to this work. Abstract: There have been no large-scale studies on the epidemiology of benign convulsions with mild gastroenteritis (CwG) since the introduction of the rotavirus vaccine in South Korea in 2007. This study aimed to analyze the trends in rotavirus gastroenteritis (RVGE) and rotavirus-associated CwG (RaCwG) after rotavirus vaccination. Further, we aimed to analyze changes in norovirus gastroenteritis (NVGE) and norovirus-associated CwG (NaCwG) using nationwide data from the Korean Health Insurance Review and Assessment Service. Between 2007 and 2019, this study analyzed children aged
Children 2021, 8, 263 2 of 12 there has been an annual increase in the rotavirus vaccination rates of South Korean infants born in 2007 (5.1%), 2008 (26.1%), 2011 (45.2%) and 2017 (85.6%) [14]. Currently, there are clinical studies on several norovirus vaccines, including oral monovalent vaccines and bivalent intramuscular vaccines [15,16]. However, there is no commercially available norovirus vaccine. Since the rotavirus vaccine was introduced, there has been an overall decrease in the prevalence of rotavirus gastroenteritis (RVGE); in contrast, the prevalence of norovirus gastroenteritis (NVGE) has annually increased and has become a major enteric virus [17–20]. However, there have been limited national epidemiological studies for rotavirus-associated CwG (RaCwG) and norovirus-associated CwG (NaCwG). This study aimed to use post-vaccination data from the National Health Insurance Review and Assessment Service (HIRA) database to determine changes in the prevalence of RVGE, NVGE, RaCwG and NaCwG, as well as seasonal changes in the ratio of RaCwG to RVGE and NaCwG to NVGE, after the introduction of the rotavirus vaccine. 2. Materials and Methods 2.1. Data Sources National Health Insurance covers the entire population of South Korea [21]; conse- quently, it contains >98% of national medical information [22]. Using the HIRA database, medical researchers can access diagnostic codes and de-identified patient medical records. This study employed the HIRA database to determine the number of patients who visited a clinic or hospital with a diagnosis of RVGE, RaCwG, NVGE and RaCwG. Subsequently, we used the mid-year population (MYP) obtained from the Korean Statistical Information Service (KOSIS) to identify changes in annual prevalence, as well as to compare the preva- lence rates over specific periods. This study was approved by the Institutional Review Board of Inha University Hospital (IRB no. 2020-01-036). 2.2. Patient Criteria We obtained medical records of patients aged
Children 2021, 8, 263 3 of 12 To analyze the effect of additional factors on the prevalence of RaCwG, RVGE, NaCwG and NVGE, the incidence of disease was separated by age, sex and season. 2.4. Analysis of the Ratio of CwG to RVGE or NVGE By calculating the ratio of RaCwG to RVGE and the ratio of NaCwG to NVGE per year, the change in the incidence of CwG patients among enteritis patients was analyzed. To analyze the effect of additional factors on the ratio of RaCwG to RVGE and the ratio of NaCwG to NVGE, we analyzed by age, sex and season. 2.5. Statistical Analysis Data analysis was performed with remote access to the HIRA database using SAS Enterprise version 9.2 (SAS Institute, Cary, NC, USA). Statistical analyses were performed using SPSS version 19.0 (IBM, Armonk, NY, USA). Using negative binomial regression anlaysis, annual prevalence changes of RaCwG, RVGE, NaCwG and NVGE and changes in prevalence according to age, sex and season were analyzed. Furthermore, using negative binomial regression analysis, not only were the annual change of the ratio of RaCwG to RVGE and the ratio of NaCwG to NVGE examined, but also the change according to age, sex and season were analyzed. Prevalence changes in periods A and B were analyzed using chi-square analysis. Statistical significance was set at p < 0.05. 3. Results 3.1. Characteristics of Patients with RVGE, RaCwG, NVGE and NaCwG Between 2007 and 2018, there were 273,898 and 35,593 patients with RVGE and NVGE, respectively. Among them, 4246 and 337 patients had RaCwG and NaCwG, respectively. Patients with RVGE (37.8%) and RaCwG (63.1%) accounted for the highest proportions in the
Children 2021, 8, 263 4 of 12 Table 1. Cont. RVGE RaCwG NVGE NaCwG Year 2007 47,173 (17.2) 501 (11.8) 1420 (4.0) 0 2008 41,619 (15.2) 518 (12.2) 1107 (3.1) 0 2009 34,556 (12.6) 327 (7.7) 513 (1.4) 0 2010 31,232 (11.4) 293 (6.7) 937 (2.6) 2 (0.6) 2011 26,843 (9.8) 419 (9.8) 1059 (3.0) 1 (0.3) 2012 20,472 (7.5) 392 (9.2) 1377 (3.9) 0 2013 18,074 (6.6) 312 (7.3) 1978 (5.5) 4 (1.2) 2014 12,778 (4.7) 282 (6.6) 2257 (6.3) 13 (3.9) 2015 12,614 (4.6) 317 (7.5) 3047 (8.6) 16 (4.7) 2016 8949 (3.2) 267 (6.3) 6767 (19.0) 71 (21.0) 2017 10,907 (4.0) 282 (6.6) 7954 (22.3) 99 (29.4) 2018 8681 (3.1) 337 (7.9) 7177 (20.2) 131 (38.9) RVGE: rotavirus gastroenteritis, RaCwG: rotavirus-associated benign convulsion with mild gastroenteritis, NVGE: Norovirus gastroenteritis, NaCwG: norovirus-associated benign convulsion with mild gastroenteritis. Values are presented as the number of patients (%). Bold to make it easier to distinguish variables. 3.2. Annual Changes in the Prevalence of RaCwG, RVGE, NaCwG and NVGE Although the rotavirus inoculation rate increased every year, the prevalence of RaCwG did not show any statistically significant change, but the prevalence of NaCwG increased by 1.790 times each year (p < 0.001) (Table 2). Furthermore, in all years of the study period, the prevalence of RaCwG was higher than that of NaCwG (Figure 1). Table 2. Negative binomial regression analysis of patients with RaCwG, patients with NaCwG and the mid-year population (MYP). RaCwG/MYP NaCwG/MYP Exp (B) 95% CI p Value Exp (B) 95% CI p Value Age
Children 2021, 8, 263 5 of 12 Figure 1. Annual changes of the prevalence of rotavirus gastroenteritis (RVGE), rotavirus-associated benign convulsion with mild gastroenteritis (RaCwG), norovirus gastroenteritis (NVGE) and norovirus gastroenteritis (NaCwG) and the vaccination rate. (a) Annual changes of the RaCwG prevalence per 100 comprising the mid-year point (MYP) (Exp(B): 0.956, p = 0.190) and NaCwG patients per 100 comprising the MYP (Exp(B): 1.790, p < 0.001). (b) Annual changes of the prevalence of RVGE (Exp(B): 0.869, p < 0.001) and NVGE (Exp(B): 1.224, p < 0.001) per 100 comprising the MYP.
Children 2021, 8, 263 6 of 12 Table 3. Negative binomial regression analysis of patients with RVGE, patients with NVGE and the MYP. RVGE/MYP NVGE/MYP Exp(B) 95% CI p Value Exp(B) 95% CI p Value Age
Children 2021, 8, 263 7 of 12 Table 4. Negative binomial regression analysis of the patients with RaCwG compared with RVGE; the patients with NaCwG compared with NVGE. RaCwG/RVGE NaCwG/NVGE Exp(B) 95% CI p Value Exp(B) 95% CI p Value Age
Children 2021, 8, 263 8 of 12 Figure 4. Seasonal between-period comparison of the ratio of RaCwG to RVGE, p = 0.298. RVGE: rotavirus gastroenteritis, RaCwG: rotavirus-associated benign convulsion with mild gastroenteritis, Period A: 2007–2012, Period B: 2013–2018. 3.5. The Prevalence of RaCwG, RVGE, NaCwG, NVGE and the Ratio of CwG to RVGE or NVGE According to Sex The prevalence of RaCwG was significantly lower in females than in males and the odds ratio was 0.921 (p = 0.007). However, the prevalence of NaCwG did not differ significantly according to sex (Table 2). The prevalence of RVGE was significantly lower in females than in males and the odds ratio was 0.846 (p = 0.004). However, the prevalence of NVGE did not show any significant difference according to sex (Table 3). The ratio of RaCwG to RVGE and the ratio of NaCwG to NVGE were not significantly different according to sex (Table 4). 3.6. The Prevalence of RaCwG, RVGE, NaCwG, NVGE and the Ratio of CwG to RVGE or NVGE According to Age The prevalence of RaCwG was decreased in all age groups from 1 to 6 years old compared to those under 1 year old (p < 0.001). Moreover, based on the age group under 1 year old, the odds ratio decreased as the age increased (Table 2). The prevalence of NaCwG was significantly higher in the age group between 1 and 2 years old compared to the age group under 1 year old (p < 0.001). However, the prevalence was significantly lower in the age group from 3 to 6 years old compared to the age group under 1 year (p < 0.001) (Table 2). The prevalence of RVGE was significantly lower in all age groups between 2 and 6 years of age compared to those under 1 year of age. As the age increased, the odds ratio for those under 1 year old decreased (Table 3). The prevalence of NVGE was significantly higher in the age group between 1 and 2 years old compared to the age group under 1 year old (p < 0.001). However, the prevalence was significantly lower in the age group from 2 to 6 years old compared to the age group under 1 year (p < 0.001) (Table 2). The ratio of RaCwG to RVGE was significantly lower in all age groups from 2 to 6 years old compared to the age group under 1 year. At this time, the odds ratio was lower as the age group increased. The ratio of NaCwG to NVGE was significantly lower in all age groups from 5 to 6 years old compared to the age group under 1 year. However, the odds ratio in the age group from 1 to 2 years was higher than that of the age group under 1 year (Table 4).
Children 2021, 8, 263 9 of 12 4. Discussion Most patients with CwG do not present with abnormal findings in the cerebrospinal fluid test, blood test and electroencephalogram. Further, there are no convulsions after im- provement of digestive symptoms; additionally, anticonvulsants are rarely required since patients show a good long-term prognosis [23]. Therefore, further tests can be avoided through early CwG diagnosis. Numerous CwG cases are accompanied by rotavirus infec- tion [10,24]. However, the incidence of norovirus, which has recently increased, is higher during winter than other seasons, which consequently affects the NaCwG prevalence. In Korea, RotaTeq®was first introduced in 2007; however, since vaccination was not mandatory, the coverage increased after several years. In our study, the RVGE prevalence decreased after the introduction of the rotavirus vaccination, which is consistent with previ- ous reports of a post-vaccination decrease in the prevalence of rotavirus enteritis [19,25,26]. In this study, vaccination affected the decrease in the RVGE prevalence. In addition, as the rotavirus vaccination rate increased, the prevalence of RaCwG decreased. However, the prevalence of RaCwG has not been declining every year. A recent study on patients with RaCwG aged
Children 2021, 8, 263 10 of 12 that urban areas have a higher RaCwG prevalence than rural areas [27]. According to the KOSIS data, there has been a gradual increase in the size of the urban population in South Korea. Therefore, factors associated with the residence of the patients may af- fect the ratio of RaCwG to RVGE and NaCwG to NVGE. Furthermore, uric acid can be used as a diagnostic index for RaCwG; therefore, the effects of uric acid on the ratio of RaCwG to RVGE should be considered [47]. The ratio of NaCwG to NVGE consistently increased regardless of rotavirus vaccination. Thus, since there was an increasing trend in the NVGE prevalence, factors other than the increased number of patients with NVGE contributed to the increased NaCwG prevalence. There are reports that a family history is associated with the occurrence of CwG, suggesting that genetic factors may influence the prevalence of CwG [48,49]. For example, there are several studies on the effect of mutations in the neuronal sodium channel alpha 1 subunit (SCN1A) gene on the pathogenesis of CwG [50–52]. During the study period, there was a continuous increasing trend in the ratio of RaCwG to RVGE; moreover, the ratio of NaCwG to NVGE showed a similar increase in the non-vaccinated norovirus group. Therefore, it can be considered that vaccination against the enteritis virus does not improve the ratio of CwG to acute gastroenteritis. This study has several limitations. First, we could not directly verify the participants’ medical records. Specifically, use of the HIRA database alone could not yield specific clinical information regarding the patients, including the type and duration of convulsion; and it was not possible to know exactly how the patient was diagnosed with rotavirus, norovirus enteritis or CwG associated with this virus. Second, diagnostic codes could be used to differentiate patients. In cases where diagnostic codes were omitted for patients with test results indicative of RVGE or NVGE, the number of patients would have been as low as those excluded from the study. Third, this study did not sufficiently consider the coinfection of rotavirus and norovirus due to technical limitations in the process of using the HIRA database. Because of this, the prevalence of each disease can be calculated higher than it actually is. Our findings revealed a decrease in the prevalence of RVGE and RaCwG after rotavirus vaccination. However, NVGE and NaCwG, which were not associated with rotavirus vaccination, showed a continuously increased prevalence. This suggests that rotavirus vaccination is effective for RVGE-caused gastrointestinal symptoms and CwG, which is related to the nervous system. Additionally, it may be helpful in differential diagnosis of seizures for clinicians to keep in mind the possibility of CwG in children under 2 years of age. There is also a need to develop a norovirus vaccine to reduce the incidence of NVGE and NaCwG. However, since the ratio of RaCwG to RVGE and NaCwG to NVGE continuously increased, further studies are required to identify other factors that increase the progression of CwG to acute gastroenteritis. Moreover, there is a need to determine whether the prevalence of CwG continues to increase overall. Author Contributions: Conceptualization: D.J.H.; Methodology: D.J.H. and Y.S.L.; Data curation: D.J.H. and M.J.C.; Formal analysis: D.H.K.; Validation: D.H.K.; Writing—original draft: Y.S.L.; Writing—review & editing: Y.S.K. All authors have read and agreed to the published version of the manuscript. Funding: This research was funded by an Inha University Hospital Research Grant. Institutional Review Board Statement: The study was conducted according to the guidelines of the Declaration of Helsinki and approved by the Institutional Review Board of Inha University Hospital (IRB no. 2020-01-036). Informed Consent Statement: Not applicable, for studies on anonymous claim database. Data Availability Statement: The data are not publicly available. Acknowledgments: The authors would like to thank all the members of the Korean Society of Pediatric Infectious Diseases and the Korean Child Neurology Society.
Children 2021, 8, 263 11 of 12 Conflicts of Interest: The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. References 1. Centers for Disease Control and Prevention. Rotavirus. In Epidemiology and Prevention of Vaccine-Preventable Diseases, 13th ed.; Hamborsky, J., Kroger, A., Wolfe, S., Eds.; Public Health Foundation: Washington, DC, USA, 2015; pp. 311–322. 2. Centers for Disease Control and Prevention. Norovirus Worldwide. December 2017. Available online: https://www.cdc.gov/ norovirus/trends-outbreaks/worldwide.html (accessed on 29 March 2021). 3. Leshem, E.; Lopman, B.A. Viral Gastroenteritis. In Principles and Practice of Pediatric Infectious Diseases, 5th ed.; Long, S.S., Prober, C.G., Fischer, M., Eds.; Elsevier: Philadephia, PA, USA, 2018; pp. 383–387. 4. Wong, V. Acute gastroenteritis-related encephalopathy. J. Child Neurol. 2001, 16, 906–910. [CrossRef] 5. Nakagomi, T.; Nakagomi, O. Rotavirus antigenemia in children with encephalopathy accompanied by rotavirus gastroenteritis. Arch. Virol. 2005, 150, 1927–1931. [CrossRef] 6. Ito, S.; Takeshita, S.; Nezu, A.; Aihara, Y.; Usuku, S.; Noguchi, Y.; Yokota, S. Norovirus-associated encephalopathy. Pediatr. Infect. Dis. J. 2006, 7, 651–652. [CrossRef] 7. Goodgame, R.W. Viral causes of diarrhea. Gastroenterol. Clin. N. Am. 2001, 30, 779–795. [CrossRef] 8. Abe, T.; Kobayashi, M.; Araki, K.; Kodama, H.; Fujita, Y.; Shinozaki, T.; Ushijima, H. Infantile convulsion with mild gastroenteritis. Brain Dev. 2000, 22, 301–306. [CrossRef] 9. Komori, H.; Wada, M.; Eto, M.; Oki, H.; Aida, K.; Fujimoto, T. Benign convulsions with mild gastroenteritis: A report of 10 recent cases detailing clinical varieties. Brain Dev. 1995, 17, 334–337. [CrossRef] 10. Kang, B.; Kwon, Y.S. Benign convulsion with mild gastroenteritis. Korean J. Pediatr. 2014, 57, 304–309. [CrossRef] 11. Lloyd, M.B.; Lloyd, J.C.; Gesteland, P.H.; Bale, J.F., Jr. Rotavirus gastroenteritis and seizures in young children. Pediatr. Neurol. 2010, 42, 404–408. [CrossRef] 12. Durá-Travé, T.; Yoldi-Petri, M.E.; Gallinas-Victoriano, F.; Molins-Castiella, T. Infantile convulsions with mild gastroenteritis: A retrospective study of 25 patients. Eur. J. Neurol. 2011, 18, 273–278. [CrossRef] [PubMed] 13. World Health Organization. Rotavirus vaccines: An update. Wkly. Epidemiol. Rec. 2009, 84, 533–540. 14. Lee, S.G.; Jeon, S.Y.; Park, K.S. Rotavirus vaccine coverage and related factors. J. Korean. Soc. Matern. Child Health 2019, 23, 175–184. [CrossRef] 15. Mattison, C.P.; Cardemil, C.V.; Hall, A.J. Progress on norovirus vaccine research: Public health considerations and future directions. Expert Rev. Vaccines 2018, 17, 773–784. [CrossRef] 16. Kim, L.; Liebowitz, D.; Lin, K.; Kasparek, K.; Pasetti, M.F.; Garg, S.J.; Gottlieb, K.; Trager, G.; Tucker, S.N. Safety and immunogenicity of an oral tablet norovirus vaccine, a phase I randomized, placebo-controlled trial. JCI Insight 2018, 3, e121077. [CrossRef] 17. Shim, J.O.; Chang, J.Y.; Shin, S.; Moon, J.S.; Ko, J.S. Changing distribution of age, clinical severity, and genotypes of rotavirus gastroenteritis in hospitalized children after the introduction of vaccination: A single center study in Seoul between 2011 and 2014. BMC Infect. Dis. 2016, 16, 287. [CrossRef] [PubMed] 18. Park, D.K.; Chung, J.Y. Changes in the outbreak of rotavirus gastroenteritis in children after introduction of rotavirus vaccines: A retrospective study at a tertiary hospital. Korean J. Pediatr. Infect. Dis. 2014, 21, 167–173. [CrossRef] 19. Payne, D.C.; Boom, J.A.; Staat, M.A.; Edwards, K.M.; Szilagyi, P.G.; Klein, E.J.; Selvarangan, R.; Azimi, P.H.; Harrison, C.; Moffatt, M.; et al. Effectiveness of pentavalent and monovalent rotavirus vaccines in concurrent use among US children
Children 2021, 8, 263 12 of 12 28. Pardo-Seco, J.; Cebey-López, M.; Martinón-Torres, N.; Salas, A.; Gómez-Rial, J.; Rodriguez-Tenreiro, C.; Martinón-Sánchez, J.M.; Martinón-Torres, F. Impact of rotavirus vaccination on childhood hospitalization for seizures. Pediatric Infect. Dis. J. 2015, 34, 769–773. [CrossRef] 29. Sheridan, S.L.; Ware, R.S.; Grimwood, K.; Lambert, S.B. Febrile Seizures in the Era of Rotavirus Vaccine. Pediatric. Infect. Dis. Soc. 2014, 5, 206–209. [CrossRef] [PubMed] 30. Lee, H.; Kim, M.; Lee, J.E.; Lim, M.; Kim, M.; Kim, J.-M.; Jheong, W.H.; Kim, J.; Ko, G. Investigation of norovirus occurrence in groundwater in metropolitan Seoul, Korea. Sci. Total Environ. 2011, 409, 2078–2084. [CrossRef] 31. Cho, H.G.; Lee, S.G.; Kim, J.E.; Yu, K.S.; Lee, D.Y.; Park, P.H.; Yoon, M.H.; Jho, E.H.; Kim, J.; Paik, S.Y. Molecular epidemiology of norovirus GII.4 variants in children under 5 years with sporadic acute gastroenteritis in South Korea during 2006–2013. J. Clin. Virol. 2014, 61, 340–344. [CrossRef] 32. Qi, R.; Huang, Y.-T.; Liu, J.-W.; Sun, Y.; Sun, X.-F.; Han, H.-J.; Qin, X.R.; Zhao, M.; Wang, L.J.; Li, W.; et al. Global prevalence of asymptomatic norovirus infection: A meta-analysis. EClinicalMedicine 2018, 2–3, 50–58. [CrossRef] 33. Chan, C.M.; Chan, C.W.; Ma, C.K.; Chan, H.B. Norovirus as cause of benign convulsion associated with gastro-enteritis. J. Paediatr. Child Health 2011, 47, 373–377. [CrossRef] 34. Chen, S.Y.; Tsai, C.N.; Lai, M.W.; Chen, C.Y.; Lin, K.L.; Lin, T.Y.; Chiu, C.H. Norovirus infection as a cause of diarrhea-associated benign infantile seizures. Clin. Infect. Dis. 2009, 48, 849–855. [CrossRef] 35. Hall, A.J.; Lopman, B.A.; Payne, D.C.; Patel, M.M.; Gastañaduy, P.A.; Vinjé, J.; Parashar, U.D. Norovirus disease in the United States. Emerg. Infect. Dis. 2013, 19, 1198–1205. [CrossRef] 36. Korea Disease Control and Provention Agency (KDCA). Infectious Diaseases Surveillance Yearbook; KDCA: Osong, Korea, 2019; pp. 28–30. 37. Gutiérrez-Aguirre, I.; Steyer, A.; Boben, J.; Gruden, K.; Poljšak-Prijatelj, M.; Ravnikar, M. Sensitive Detection of Multiple Rotavirus Genotypes with a Single Reverse Transcription-Real-Time Quantitative PCR Assay. J. Clin. Microbiol. 2008, 45, 2547–2554. [CrossRef] [PubMed] 38. Soltan, M.A.; Tsai, Y.-L.; Lee, P.-Y.A.; Tsai, C.-F.; Chang, H.-F.G.; Wang, H.-T.T.; Wilkes, R.P. Comparison of electron microscopy, ELISA, real time RT-PCR and insulated isothermal RT-PCR for the detection of Rotavirus group A (RVA) in feces of different animal species. J. Virol. Methods 2016, 235, 99–104. [CrossRef] [PubMed] 39. Park, S.H.; Kim, Y.O.; Kim, H.K.; Kim, H.S.; Kim, B.Y.; Cheon, K.R.; Kim, M.J.; Kim, S.H.; Chung, J.K.; Woo, Y.J. Incidence of benign convulsions with mild gastroenteritis after introduction of rotavirus vaccine. Brain Dev. 2015, 37, 625–630. [CrossRef] [PubMed] 40. Cho, H.; Lee, H.; Kim, D.S.; Kim, H.M.; Kim, J.H.; Kim, A.Y.; Kang, H.Y. Socioeconomic impact of the rotavirus vaccine in Korea: Comparing the epidemiologic and economic characteristics of rotavirus gastroenteritis before and after the introduction of vaccines. Pediatr. Infect. Dis. J. 2020, 39, 460–465. [CrossRef] 41. Hung, J.J.; Wen, H.Y.; Yen, M.H.; Chen, H.W.; Yan, D.C.; Lin, K.L.; Lin, S.J.; Lin, T.Y.; Hsu, C.Y. Rotavirus gastroenteritis associated with afebrile convulsion in children: Clinical analysis of 40 cases. Chang Gung Med. J. 2003, 26, 254–259. 42. Hungerford, D.; Jere, K.C.; Bar-Zeev, N.; Harris, J.P.; Cunliffe, N.A.; Iturriza-Gómara, M. Epidemiology and genotype diversity of norovirus infections among children aged
You can also read